Failure of a Best Practice Alert to Reduce Antibiotic Prescribing Rates for Acute Sinusitis Across an Integrated Health System in the Midwest

BACKGROUND: Antimicrobial resistance is a growing concern, and in recent years, there has been increased interest in ambulatory antimicrobial stewardship. Acute rhinosinusitis (ARS) is one of the most common outpatient diagnoses that results in an antibiotic prescription. OBJECTIVE: To determine if a best practice alert (BPA) will affect the percentage of oral antibiotic prescriptions for adults with ARS. METHODS: A prospective, pre/post study was initiated to evaluate the percentage of oral antibiotic prescriptions for ARS in 117 primary care clinics in the Midwest. Included in the study results were 16,570 adults who had an office visit for ARS: 8,106 patients from December 1, 2015, to February 28, 2016, were in the pre-intervention group without an active BPA, and 8,464 patients from December 1, 2016, to February 28, 2017, were in the post-intervention group when the BPA was active. The primary outcome was the number of oral antibiotic prescriptions for ARS compared with the number of office visits for ARS in the pre- and postintervention groups. RESULTS: The percentage of oral antibiotics prescribed for the pre- and postintervention groups were 94.8% and 94.3%, respectively (P = 0.152). The BPA displayed for 7,780 visits, prompting discontinuation of an antibiotic for 10 (0.1%) visits in the postintervention group. CONCLUSIONS: This study suggests that, although an electronic alert may be attractive to facilitate antimicrobial stewardship, it may be ineffective. These results warrant alternative measures to facilitate ambulatory antimicrobial stewardship.

A cute rhinosinusitis (ARS) is a common respiratory illness with over 30 million diagnoses in the United States each year, of which 80% of cases receive antibiotic prescriptions. 1,2 Direct costs associated with the management of sinusitis in the United States surpasses $11 billion annually. 3 Although ARS is the fifth most common diagnosis resulting in an antibiotic prescription, clinical guidelines recommend antibiotic therapy only if signs and symptoms are persistent for 10 or more days; are severe for at least 3-4 days (e.g., fever ≥ 39 o C and purulent nasal discharge or facial pain); or worsen after initial improvement (double sickening). [3][4][5] An important modifiable risk factor for antibiotic resistance is reducing the number of inappropriate antibiotic prescriptions. 6 Over 60% of antibiotic expenditures are associated with the outpatient setting, where overprescribing of antibiotics has been suggested. 7,8 Available data indicate that over 30% of outpatient antibiotic prescriptions in the United States may be inappropriate, and in ARS, it may be closer to 50%. 8 Given that antibiotic use is a driving factor for antibiotic resistance, 6 antimicrobial stewardship efforts should target common diagnoses, such as ARS, that often result in antibiotic use.
Reducing inappropriate antibiotic prescriptions for sinusitis represents an opportunity for quality improvement in the era of evidence-based practice. Aligning with recent sinusitis guidelines, a recommendation for reducing low-value care by the American Academy of Family Physicians' Choosing Wisely is to avoid routine prescribing of antibiotics for acute mild-tomoderate sinusitis. 4,9 The use of best practice alerts (BPAs) is • The majority of antibiotic expenditures are associated with the ambulatory setting, and a modifiable risk for reducing antibiotic resistance is reducing inappropriate antibiotic prescriptions. • Acute rhinosinusitis (ARS) is a common ambulatory diagnosis that often results in an antibiotic prescription, and treatment guidelines recommend to withhold antibiotics in mild-to-moderate ARS and those with a symptom duration of less than 10 days. • Best practice alerts (BPAs) are automated alerts within the electronic medical record that help facilitate widespread communication of information to primary care providers and may be used as a tool for an antimicrobial stewardship strategy.

What is already known about this subject
• This study explored the feasibility of using a BPA as an antimicrobial stewardship tool to reduce inappropriate antibiotic prescribing in ARS. • Results suggest that this BPA was ineffective in reducing inappropriate antimicrobial prescribing in ARS. • The BPA prompted the removal of an antibiotic prescription during a patient encounter; however, this action was largely dismissed by providers, and prescribing habits of providers did not change throughout the intervention period. A real-time BPA was implemented in the electronic medical record to notify the provider of the Choosing Wisely becoming a common strategy to provide real-time clinical decision support and steer clinicians towards providing evidencebased care. 10 Our institution implemented an electronic intervention in an effort to reduce the use of antibiotics for ARS. The objective of this study was to measure the effect of a BPA on the percentage of antibiotic prescribing for ARS.

■■ Methods
This study included office visits for ARS at 117 acute care (defined as urgent care and walk-in), family medicine, and internal medicine clinics that represented 615 providers within an integrated health system in the Midwest (Iowa, Minnesota, North Dakota, and South Dakota). We conducted a quasiexperimental pre/post study that evaluated the proportion of ARS clinic visits resulting in an oral antibiotic prescription. Diagnoses used for patient exclusion were adapted from a previous study by Meeker et al. (2016), which evaluated antibiotic prescribing for acute respiratory tract infections. 11 Visits were excluded if patients had medical comorbidities, which included any of the following: Do not routinely prescribe antibiotics for acute mild to moderate sinusitis unless symptoms last for 7 or more days or symptoms worsen after initial clinical improvement.

American Academy of Family Physicians American College of Emergency Physicians Information for Patients
Recommendation: Patient has an antibiotic order placed in this encounter. If the antibiotic order was placed for the visit diagnosis of sinusitis, consider removing it.
Remove the following orders? ____________________________________________________________________________________________  Failure of a Best Practice Alert to Reduce Antibiotic Prescribing Rates for Acute Sinusitis Across an Integrated Health System in the Midwest recommendation when prescribing an antibiotic for a patient diagnosed with ARS during that visit (Figure 1). A diagnosis of sinusitis triggered a pop-up screen with a link to the Choosing Wisely recommendation and a prompt to remove the antibiotic prescription. 9 Optional justification for continuing the antibiotic order, designated as "acknowledgement reasons," could be selected in the BPA response field. One of six discrete acknowledgment reasons, as developed by a physician-led clinical decision support committee, could be selected or entered as free text. The alert could be dismissed without requiring the clinician to provide justification for the antibiotic prescription. The BPA began displaying to providers 6 weeks before the 3-month intervention period during peak winter months (December 2016-February 2017). Data from this period were compared with the same months the previous year (December 2015-February 2016) to minimize any confounding effect of seasonal variation. Data collected included baseline characteristics, oral antibiotics prescribed during office visits, antibiotic recommendation category for ARS (first line, second line, other), and provider responses to the BPA (Table 1). Department types in the study included acute care, family medicine, and internal medicine departments.
In this study, we categorized first-line antibiotics as amoxicillin or amoxicillin-clavulanate; second-line antibiotics as second-or third-generation cephalosporins, clindamycin, doxycycline, levofloxacin, moxifloxacin, or minocycline; and other antibiotics were those not recommended because of high rates of resistance to S. pneumoniae or lack of appropriate bacterial coverage. 3,4 The primary outcome was the number of oral antibiotic prescriptions for ARS compared with the number of office visits for ARS in the pre-and postintervention groups. The difference in the percentage of antibiotics prescribed between the pre-and postintervention groups was tested using Pearson's chi-square test. Secondary outcomes included the same evaluation across subgroups and postintervention months ( Table 1). The data were analyzed with JMP software, version 12.0.0 (SAS Institute, Cary, NC). A P value of < 0.05 was considered statistically significant. This work was reviewed by the Sanford Health Institutional Review Board and was determined to be quality improvement rather than human subjects research.

■■ Results
In the pre-intervention group, there were 14,566 unique patient visits, with 8,106 eligible for inclusion. In the postintervention group, there were 14,092 unique patient visits, with 8,464 eligible for inclusion. Results based on baseline characteristics are summarized in Table 1. Antibiotics were prescribed in 94.8% of sinusitis visits in the pre-intervention group, and 94.3% of sinusitis visits in the postintervention group (P = 0.152). The overall percentage of oral antibiotic prescriptions based on department type for acute care, family medicine, and internal medicine were 97.2%, 93.2%, and 86.0%, respectively (P < 0.001).
The BPA displayed for 7,780 visits, prompting discontinuation of an antibiotic in 10 (0.1%) visits in the postintervention group. During the postintervention period, the percentage of oral antibiotics prescribed for the months of December 2016, January 2017, and February 2017 were 94.5%, 94.5%, and 94.1%, respectively (P = 0.749).
A multivariable logistic regression analysis was performed to adjust for potential confounding variables related to whether an antibiotic was prescribed during the entire study time frame. The model included the presence of the BPA, age, insurance type, provider type, clinic type, and the following comorbidities: hypertension, heart failure, ischemic heart disease, diabetes mellitus, chronic kidney disease, and depressive disorder. The only independent predictors of an antimicrobial

Patient Characteristics and Antibiotic Prescriptions According to Subgroup (continued)
Failure of a Best Practice Alert to Reduce Antibiotic Prescribing Rates for Acute Sinusitis Across an Integrated Health System in the Midwest prescription were a visit in the acute care department (P < 0.001) and increasing age as a continuous variable (P < 0.001). Being in the BPA group was not associated with decreased odds of an antimicrobial prescription in the adjusted model (P = 0.125). Among the subgroups, only the acute care department demonstrated a statistically significant difference in the rate of antimicrobial prescribing (97.9% pre-intervention vs. 96.5% postintervention, P < 0.001). In the age subgroup analyses, patients were divided into 4 age cohorts (18-44 years, 45-64 years, 65-74 years, and 75 years or older), none of which demonstrated statistically significant changes in antimicrobial prescriptions after BPA implementation.

■■ Discussion
Ninety-four percent of patients received an antibiotic if they were seen within our health system for ARS, while national prescribing rates are closer to 80%. Given that an estimated 2%-10% of ARS cases are caused by bacteria, 12 the large percentage of antibiotic prescriptions for ARS suggests probable overprescribing. This BPA was implemented to decrease inappropriate antibiotic prescribing but was largely dismissed by providers, and the percentage of oral antibiotics prescribed for ARS was unaffected.
The majority of office visits for ARS were seen by acute care or family medicine providers, encompassing 96.3% of overall visits in this study, with 3.7% of office visits occurring at internal medicine clinics. The baseline characteristic analyses demonstrated some statistical differences in age, provider type, insurance, and comorbidities (Table 1). However, no differences in antibiotic prescribing were demonstrated in any of these subgroups. The only subgroup found to have a statistical difference in antibiotic prescribing was acute care. Whether the BPA was actually more effective in changing prescribing behavior in the acute care setting is uncertain because of the low absolute decrease in antimicrobial prescriptions (1.4%).
After adjusting for baseline characteristic differences in a multivariable model, the presence of the BPA was not associated with decreased odds of receiving an antimicrobial prescription (Table 1). Our finding related to acute care visits being statistically associated with increased antimicrobial prescriptions over the entire study time frame is pragmatic and likely reflects severity of illness. Primary care specialties have been associated with overall higher rates of antibiotic prescribing, particularly in family medicine compared with internal medicine practices. 13 Higher prescribing rates within acute care and family medicine departments may be related to pressure from patients, the need to achieve quicker outcomes, or lack of follow-up to ensure symptom resolution, since this visit may not have occurred with the patient's primary provider.
The percentage of ARS visits that resulted in antibiotic prescriptions by physicians, nurse practitioners, and physician assistants were similar. Nurse practitioners and physician assistants have been associated with higher antibiotic prescribing rates in respiratory tract infections compared with physician-only visits, with minimal difference in the prescribing practices between nurse practitioners and physician assistants. 14 Our results show that ambulatory antimicrobial stewardship efforts should target all providers rather than focusing only on advanced practice providers.
First-line antibiotic prescribing increased 7.1% from the pre-intervention group to the postintervention group, reaching 57%. Second-line antibiotic use did not change between the 2 periods, but use of other antibiotics decreased during the intervention period. In the United States, the prescribing rate of first-line antibiotics for ARS has been reported near 37%, with the majority of patients receiving non−first-line antibiotics. 15 The higher percentage of first-line antibiotic prescribing in our study could be related to its exclusion criteria, which omitted patients with comorbid conditions that may have otherwise elicited more broad-spectrum antibiotic use. The reasons that higher first-line antibiotic use was found in the postintervention group are unclear, since antibiotic selection was not an aim of the intervention. It is possible the BPA coincidentally increased provider vigilance in antibiotic selection, prompting use of narrower-spectrum or guideline-concordant agents.
Although an electronic alert is a common intervention strategy to guide a provider's practice, it may be judicious to trial and validate its effect before deployment across a health system. When incorporating electronic alerts in the workflow of front-line providers, challenges remain in providing the proper balance of actionable information and dismissal mechanisms. 16 If a BPA is used as an antimicrobial stewardship strategy, consideration should be given to its use as part of a multifaceted intervention rather than a stand-alone tool.

Limitations
This study has limitations that need to be considered. First, the control group was a historical cohort, so the observed intervention effect may be biased by other factors that affected the percentage of antibiotics prescribed. Similar to other investigations of this nature, we were unable to capture how many patients had a true indication for an antibiotic, since the BPA simply served to remind the clinician of best practices. Our proportion of prescribing, however, suggested a substantial degree of inappropriate prescribing in the pre-and postintervention groups.
The study time frame included only a portion of the influenza season. Since data were not collected throughout its continuum (usually regarded as October through March 17 ), the